Inhibition of return

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Raymond M. Klein and Jason Ivanoff (2008), Scholarpedia, 3(10):3650. doi:10.4249/scholarpedia.3650 revision #90806 [link to/cite this article]
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Inhibition of return (IOR) refers to the relative suppression of processing of (detection of, orienting toward, responding to) stimuli (object and events) that had recently been the focus of attention. By suppressing orienting toward previously inspected locations and objects, IOR encourages orienting toward novelty (Posner & Cohen, 1984) and consequently can serve as a search or foraging facilitator (Itti & Koch, 2001; Klein, 1988; Klein & MacInnes, 1999). To understand how IOR may perform this function and how its properties have been studied, it is useful to introduce the concept of selective attention and the cuing paradigm that has been used so fruitfully to explore attentional orienting.

Our environment is far too complex for us to process fully and simultaneously all the information it provides. Selective attention is a phrase used to describe the consequence of this limitation. To paraphrase William James, “we must withdraw from some sources of information in order to deal more effectively with others.” How does selective attention operate? Because so much work has been done to answer this question in the visual modality, we will begin with the everyday example of searching a scene for something, such as looking for a friend's face in a crowd of people. Scholars who have developed computational models of such a search process have hypothesized a “saliency map” within which activity is based on the convergence of bottom-up feature extraction and top-down signals defining one’s goal (i.e., the friend's face, called the target) and reflecting stored information that may be relevant to the visual search. A “winner-take-all” selection algorithm (see Figure 1)
Figure 1: Model of visual search based on Itti and Koch (2001). Visual input reaches the retina and attentional processes create a saliency-based feature map. Items in the visual array are initially selected via a winner-take-all mechanism. Rejected items are tagged by IOR until the target item (i.e., the first author of this paper) is selected.
causes the most activated object or location in the scene to capture attention. When this item is not the target the search continues until the target is found. But without a mechanism to reduce the salience of the just-inspected item, it will remain the most salient, the selection algorithm will perseverate, and the search will fail. It has been proposed that Inhibition of Return, which was first observed by Posner and Cohen (1984) in the simple cuing experiment described in the next section, might perform this function (Itti & Koch, 2001; Klein, 1988).


Exogenous Cueing

In a typical exogenous cueing paradigm (Fig. 2a), a peripheral, spatially non-informative, stimulus (i.e., the cue) precedes the presentation of a target stimulus that requires detection, identification or discrimination. The cue may be any sort of salient event, (e.g. the appearance of a new object) that captures attention, and reflecting this capture, responses to targets are faster to cued targets (i.e., those targets occupying space previously occupied by the cue) than to uncued targets (i.e., targets appearing at a new location) when the cue-target onset asynchrony (CTOA; i.e., the time interval between the onset of the cue and target) is less than ~250ms. This facilitative effect of the cue for targets at the cued vs uncued locations has been attributed the benefit of attention being at the location of cued targets and the cost of having to reorient attention away from cued locations toward uncued targets. When the cue is uninformative about the location of the target the capture of attention by the cue is transient. Indeed, in 1984, Posner and Cohen discovered that when the CTOA is increased beyond 250ms, this facilitative effect reverses and responses to cued targets become slower than responses to uncued targets (Fig. 2b). This latter effect of the cue has been called inhibition of return (IOR), a name for the phenomenon first used by Posner, Rafal, Choate & Vaughan (1985) that also suggests a theoretical mechanism: After attention has been removed from a location, it is inhibited from returning to that location. Despite some challenges to this description of the mechanism of IOR, the IOR effect is robust and the novelty-seeking function described here is well-established.
Figure 2: a) Typical cueing task used to generate and measure inhibition of return (IOR). b) Results from Posner and Cohen’s (1984) study that first revealed IOR.

Foreshadowing the proposal described in the first paragraph, Posner and Cohen suggested that the function of inhibition of return is to encourage orienting to novel objects and events. To perform this function (suppressing the activation level of recently inspected regions of the saliency map) IOR requires the following properties: it should be local (confined to a relatively specific area of space); it should be coded in environmental and object coordinates (so it can survive scanning eye movements and movements of objects in the search array); it should be initiated rapidly enough and last long enough to be useful in a typical search episode; and it should be able to tag multiple items or locations. The exogenous cuing paradigm has proved to be flexible enough to characterize IOR on each of these dimensions.

Spatial Extent of IOR

Using two vertical arrays of cue and target locations, Maylor and Hockey (1985) found that IOR was greatest at the cued location and showed a decreasing gradient as the distance between the cued location and the target increased. Bennett and Pratt (2001) presented one of four cues (one in each quadrant) and then placed a target at any of 410 locations. They found that IOR was greatest at the cued location, and gradually became weaker as targets were presented further from the cue; see also Berlucchi, Tassinari, Marzi & Di Stefano (1989); Klein, Christie & Morris (2005). Thus, IOR is local and graded.

Environmental- and Object-based IOR

During a natural search for objects in the real world, we make eye movements to bring regions we need to inspect into the high resolution fovea and objects that we inspect may move to new locations after we have determined they are not the target. If IOR were simply coded in retinotopic coordinates, it would be unable to discourage reorienting in the face of eye movements or movements of objects in the scene.

By interposing an eye movement between the cue and the appearance of the target, Posner and Cohen (1984), and later Maylor and Hockey (1985), demonstrated that IOR could be coded in environmental (rather than retinotopic) coordinates. In both studies it was the location in space that had been stimulated that was inhibited, and not the location on the retina that had been stimulated.

The first evidence that IOR could be tagged to objects came from a modified cueing task. Tipper, Driver, and Weaver (1991) presented 3 squares along the horizontal axis (Figure 3). One of the outer two squares was briefly cued before both squares began to move clockwise along the path of an imaginary circle. The central square remained stationary. When the motion stopped, RTs to targets were slowed at the location of the cued object even though, because of the motion, this location had not originally been cued. Tipper, Jordan, and Weaver (1999) later found IOR at both the original location of the cue and the location of the cued object after motion. The relative magnitudes of the IOR effects were affected by the level of integration of the scene elements (with greater object-based IOR with more integrated scenes).
Figure 3: Graphic illustration of the task used by Tipper and colleagues to isolate and study object-based IOR.

If IOR is tagged to objects, then it should quickly spread across the surface of an object when attention is removed from only part of it. Jordan and Tipper (1999) examined whether IOR extended to uncued regions of a cued object. Two rectangles were presented. One end of a rectangle was cued. Targets could appear at the cued location within the rectangle, at the uncued location within the rectangle, or within the other, uncued rectangle. Responses were slowest at the cued location within the rectangle, but they were also slowed at the uncued location within the cued rectangle (see also Repp & Leek, 2003).

The parietal lobe has been linked to both environmental and object-based IOR. Sapir and colleagues (Sapir, Hayes, Henik, Danziger, & Rafal, 2004) reported that patients with damage to the right parietal lobe present IOR in retinal, but not environmental, co-ordinates suggesting that the right parietal lobe plays a role in the environmental coding of inhibitory tags. Vivas, Humphreys, & Fuentes (2008) reported that patients with unilateral parietal lesions failed to show IOR when objects were cued in the contralesional field and then moved towards the ipsilesional field. On the other hand, object-based IOR was expressed normally in the opposite direction (ipsilesional to contralesional). Thus the parietal lobe seems to play a crucial role in higher-level facets of IOR.

The chronometry of IOR

If IOR were to serve a role in search, it should be expressed once a distractor has been inspected and rejected. The timecourse of IOR in a typical cuing paradigm (see Fig. 2) seems, at first glance, a little slow for it to be useful in search (Horowitz & Wolfe, 2005) where hypothetical inspections take place many times per second (see Visual search). We say “at first glance” because neuroscientific evidence (see Klein, 2004, for a discussion) suggests that IOR begins with the cue. When combined with performance data like those illustrated in Figure 2 this suggests that IOR is overshadowed in a cuing task by facilitation due to attentional capture. In support of this view, when attention is encouraged to disengage rapidly from a cue (Danziger & Kingstone, 1999; Dodd & Pratt, 2007), IOR can be apparent within 50 ms of the cue’s appearance. Whereas the view that IOR begins when attention disengages from an exogenously attended location had been widely held, there is now strong evidence that IOR from a peripheral cue can be seen at a location that is presently attended endogenously (e.g., Berlucchi, Chelazzi & Tassinari, 2000; Lupiáñez, Decaix, Sieroff, Chokron, Milliken, & Bartolomeo, 2004). Once it is accepted that IOR and facilitation due to attention can co-exist at the same location (see Klein, 2000, Box 1) the aforementioned meaning of the term “inhibition of return,” which implies that attention has left the cued object or location, is challenged. One answer to this challenge is to consider the IOR effect as habituation of the orienting reflex (Dukewich, in press). This way, while operating on the salience map that controls orienting, the IOR effect can co-exist with attentional and other processes that might speed or delay response times.

Does IOR last long enough to be useful in preventing re-inspections in a typical search episode? Studies exploring this question support the conclusion that IOR typically lasts for at least 3 seconds (see review by Samuel & Kat, 2003).

The Causes and Effects of IOR

Our understanding of the role of IOR in search processes would clearly be extended if we understood how IOR slows responding (i.e., the effects of IOR) and how it operates (i.e., the cause of the IOR). Only by considering both can we truly appreciate its functional significance. Moreover, as noted by Taylor and Klein (1998), for IOR to be observed in a cue-target task two conditions must be satisfied: The cue must have caused IOR and the task performed on the target must be sensitive to IOR’s effects. In addition, the negative impact of IOR on performance must exceed any facilitatory effects that might be present when the target is presented.

Causes of IOR

IOR follows the facilitation associated with attentional capture by an event in the periphery but it does not follow a voluntary shift of attention (Posner & Cohen, 1984; Rafal, Calabresi, Brennan, & Sciolto, 1989) in the absence of peripheral stimulation. Because peripheral stimulation automatically activates the oculomotor system while a voluntary shift of attention in the absence of eye movements does not (Klein, 1980; Klein & Pontefract, 1994), this pattern of results suggests that what generates IOR is peripheral stimulation, oculomotor activation, or both. Two key findings favors oculomotor activation. First, Rafal et al. (1989) used a central arrow to get their participants to prepare an eye movement. When this oculomotor preparation was cancelled, they found IOR at the to-be-fixated location. In this case, there was no peripheral stimulus. Second, when a cue stimulated multiple locations, Klein, Christie & Morris (2005) found IOR in the net direction of a cue whether or not the target fell on a stimulated location. Moreover, when the cues’ elements were balanced around fixation (such that the net vector of the cue was zero) no IOR was observed.

Effects of IOR

While there is solid evidence showing that IOR reduces perceptual sensitivity (signal to noise ratio) (Cheal & Chastain, 1999; Handy, Jha, & Mangun, 1999; Ivanoff & Klein, 2006), there is also solid evidence demonstrating that IOR biases performance against responding to stimuli from the cued location (Ivanoff & Klein, 2001, 2004, 2006; Ivanoff, Klein, & Lupiáñez, 2002; Ivanoff & Taylor, 2006; Taylor, 2007; Taylor & Ivanoff, 2003). Both of these effects may contribute to the proposed role of IOR as a search facilitator. A signal-to-noise ratio reduction applied to previously attended objects or regions of a scene is one way to ensure that the initially most salient region of the scene might not continue to have this status. When this is insufficient, a bias against orienting toward previously attended objects or regions would be a good backup system.

Several neuroimaging techniques have been used to explore the effects of IOR. A number of studies have observed negative effects of IOR on an ERP component thought to reflect sensory processes, the P1 (McDonald, Ward, & Kiehl, 1999; Prime & Ward, 2006; Wascher & Tipper, 2004). While motoric ERP components (i.e., the lateralized readiness potential; LRP) are delayed by IOR, they do not seem to be directly affected by IOR (Prime & Ward, 2004, 2006). Thus, the ERP evidence offers support for a perceptual/attentional locus of the IOR effect.

While ERPs have excellent temporal resolution, they have notoriously poor spatial resolution, thus they do not reliably inform us about the neural locus of IOR. Although functional magnetic resonance imaging (fMRI) is a technique better suited to isolating the location of the effects of IOR, it is difficult to study IOR directly with fMRI because cue and target events are difficult to distinguish with the sluggish BOLD signal. Nevertheless, some event-related approaches offer some promise. Müller and Kleinschmidt (2007), for example, identified regions of visual cortex that passively respond to stimulation in the upper and lower visual fields to isolate early visual regions that responded to these particular locations. Following this passive localizer task, the cue and target stimuli were presented in the same locations. Although it is impossible to dissociate the cue from the target in this task the dynamics of the BOLD signal suggest that attentional facilitation increases, while IOR decreases, sensory representation in visual cortex. Thus, the fMRI evidence converges with the ERP evidence in suggesting that IOR has a suppressive effect on sensory processing and localizes this effect to processing in visual cortex.

Recording from single neurons in the intermediate layers of the monkey superior colliculus (SC), Dorris et al. (2002) observed a greatly reduced sensory response to targets presented at a previously cued as compared to a previously uncued location. Residual, cue-related activity was not suppressed, and when saccades were generated by electrical stimulation through the recording electrode, the latency of these saccades was faster when the cued region was stimulated. These findings demonstrate that after a cue, the cued region of the SC is not itself inhibited but rather is receiving inputs whose sensory responses are already reduced. Whereas the ERP and fMRI evidence point strongly to a sensory locus of the IOR effect, motoric processes are not completely unaffected by IOR. In contrast to the LRP data, which do not offer strong evidence to support a motoric effect of IOR, recent EEG analysis of beta synchrony in motor areas suggests that response processes do play a crucial role in IOR (Pastötter, Hanslmayr, & Bauml, 2008). Interestingly, these EEG metrics of IOR correlate strongly with the behavioral measure of IOR. The discrepancy between these two methods may depend on what information processing mechanisms each is sensitive to. We believe that the LRP may be sensitive to pre-activation of one response over another while the beta synchrony may be sensitive to the degree to differences in decision criterion to respond. Altogether, then, the neuroscience evidence provides strong evidence for a motoric and for a perceptual locus of the IOR effect.

IOR in Search

In 1988, Klein tested the foraging facilitator proposal by probing for IOR following a difficult (serial) search task, one whose elements (either individually or in groups) must be inspected to determine whether or not they are the target. Following the presentation of either a parallel (easy) or serial search display, a probe was presented at a location occupied by a distractor or a previously empty location. If IOR was present in the display, tagging rejected distractors, then responses to the probe ought to be longer when the probe was previously occupied by a distractor, but only following serial search. This is precisely what Klein (1988) observed. This pattern was later replicated (Müller & Mühlenen, 2000; Takeda and Yagi, 2000) who showed that the inhibitory tags were removed when the search array was removed prior to the presentation of the probe (as if the tags were not spatial per se, but were stored with the representation of the scene).

Klein and MacInnes (1999) recorded eye movements while viewers searched through a complex scene (i.e., “Where’s Waldo” by Martin Handford). During the search, the viewer’s search task (they were looking for Waldo or the Wizard) was interrupted by the appearance of a probe either at a recently fixated location or at a new location. Klein and MacInnes discovered that oculomotor probe-localization responses were slower when the probe appeared at a previously fixated location. Using a “search the tree for fruit” task, Thomas et al (2006) had participants touch leaves with a virtual wand and then look behind them for target fruits. Replicating Klein & MacInnes’s finding, their participants were then slower to detect the movement of previously inspected leaves compared to new ones. In addition, eye movements during search were more likely to go in a new direction than back in the direction of the previous fixation. Thus, IOR appears to bias orienting even in more naturalistic search tasks involving eye movements (see also Sogo & Takeda, 2006, who showed that saccades during search curve away from previously fixated objects). McCarley et al. (2003), using a gaze-contingent task in which the initial sequence of fixations was controlled by the experimenter in a “follow the dots” type of task, found evidence that re-inspections were unlikely for recently attended location. In their task, a saccade to a location would allow visual inspection of an occluded search display. When given the choice between saccading to a new location versus an old location, participants more frequently chose the new location, especially when the old location had been more recently attended.

These findings, along with others discussed herein, support Posner & Cohen’s proposal that IOR functions to encourage orienting toward novel items, and Klein’s extension of this idea of IOR as a foraging facilitator in real-world search behavior. The role of IOR in search is not absolute: it does not prevent re-inspections. Rather, IOR operates to decrease the likelihood that a previously inspected (possibly salient) item in the visual scene will be re-inspected, thereby encouraging attention towards the next salient item (Itti & Koch, 2001).


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